One of the key challenges linked with future food and nutritional security is to evaluate the interactive effect of climate variables on plants' growth, fitness, and yield parameters. These interactions may lead to unique shifts in the morphological, physiological, gene expression, or metabolite accumulation patterns, leading to an adaptation response that is specific to future climate scenarios. To understand such changes, we exposed spring wheat to 7 regimes (3 single and 4 combined climate treatments) composed of elevated temperature, the enhanced concentration of CO2, and progressive drought stress corresponding to the predicted climate of the year 2100. The physiological and metabolic responses were then compared with the current climate represented by the year 2020. We found that the elevated CO2 (eC) mitigated some of the effects of elevated temperature (eT) on physiological performance and metabolism. The metabolite profiling of leaves revealed 44 key metabolites, including saccharides, amino acids, and phenolics, accumulating contrastingly under individual regimes. These metabolites belong to the central metabolic pathways that are essential for cellular energy, production of biosynthetic pathways precursors, and oxidative balance. The interaction of eC alleviated the negative effect of eT possibly by maintaining the rate of carbon fixation and accumulation of key metabolites and intermediates linked with the Krebs cycle and synthesis of phenolics. Our study for the first time revealed the influence of a specific climate factor on the accumulation of metabolic compounds in wheat. The current work could assist in the understanding and development of climate resilient wheat by utilizing the identified metabolites as breeding targets for food and nutritional security.

Department of Agrosystems and Bioclimatology Faculty of AgriSciences Mendel University in Brno Brno Czechia

Department of Forest Ecology Faculty of Forestry and Wood Technology Mendel University in Brno Brno Czechia

Laboratory of Ecological Plant Physiology Global Change Research Institute of the Czech Academy of Sciences Brno Czechia

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Agostini-Costa S., da T., F. R., R. H., Silveira D. (2012). “Secondary metabolites,” in Chromatography and its applications (London, UK: InTech; ). XXXA., M. doi: 10.5772/35705 DOI

Ainsworth E. A. (2008). Rice production in a changing climate: A meta-analysis of responses to elevated carbon dioxide and elevated ozone concentration. Global Change Biol. 14, 1642–1650. doi: 10.1111/j.1365-2486.2008.01594.x DOI

Ainsworth E. A., Rogers A. (2007). The response of photosynthesis and stomatal conductance to rising [CO2]: Mechanisms and environmental interactions. Plant Cell Environ. 30, 258–270. doi: 10.1111/j.1365-3040.2007.01641.x PubMed DOI

Aiqing S., Somayanda I., Sebastian S. V., Singh K., Gill K., Prasad P. V. V., et al. . (2018). Heat stress during flowering affects time of day of flowering, seed set, and grain quality in spring wheat. Crop Sci. 58, 380–392. doi: 10.2135/cropsci2017.04.0221 DOI

Alamri S., Siddiqui M. H., Mukherjee S., Kumar R., Kalaji H. M., Irfan M., et al. . (2022). Molybdenum-induced endogenous nitric oxide (NO) signaling coordinately enhances resilience through chlorophyll metabolism, osmolyte accumulation and antioxidant system in arsenate stressed-wheat (Triticum aestivum l.) seedlings, environmental pollution, Vol. 292. 269–7491. doi: 10.1016/j.envpol.2021.118268 PubMed DOI

Awasthi R., Bhandari K., Nayyar H. (2015). Temperature stress and redox homeostasis in agricultural crops. Front. Environ. Sci. 3. doi: 10.3389/fenvs.2015.00011 DOI

Chavan S. G., Duursma R. A., Tausz M., Ghannoum O. (2019). Elevated CO2 alleviates the negative impact of heat stress on wheat physiology but not on grain yield. J. Exp. Bot. 70, 6447–6459. doi: 10.1093/jxb/erz386 PubMed DOI PMC

Chen J., Hu X., Shi T., Yin H., Sun D., Hao Y., et al. . (2020). Metabolite-based genome-wide association study enables dissection of the flavonoid decoration pathway of wheat kernels. Plant Biotechnol. J. 18, 1722–1735. doi: 10.1111/pbi.13335 PubMed DOI PMC

Das A., Rushton P., Rohila J. (2017). Metabolomic profiling of soybeans (Glycine max L) reveals the importance of sugar and nitrogen metabolism under drought and heat stress. Plants. 6, 21. doi: 10.3390/plants6020021 PubMed DOI PMC

Fàbregas N., Fernie A. R. (2019). The metabolic response to drought. J. Exp. Bot. 70, 1077–1085. doi: 10.1093/jxb/ery437 PubMed DOI

Fang C., Fernie A. R., Luo J. (2019). Exploring the diversity of plant metabolism. Trends Plant Sci. 24, 83–98. doi: 10.1016/j.tplants.2018.09.006 PubMed DOI

Curtis B. C., Rajaram S. (2002). Bread wheat: Improvement and production,”. (Rome: Food and Agriculture Organization of the United Nations; ), 554.

Farooq M., Hussain M., Siddique K. H. M. (2014). Drought stress in wheat during flowering and grain-filling periods. Crit. Rev. Plant Sci. 33, 331–349. doi: 10.1080/07352689.2014.875291 DOI

Fernández-Gómez J., Talle B., Tidy A. C., Wilson Z. A. (2020). Accurate staging of reproduction development in cadenza wheat by non-destructive spike analysis. J. Exp. Bot. 71, 3475–3484. doi: 10.1093/jxb/eraa156 PubMed DOI PMC

Fernie A. R., Carrari F., Sweetlove L. J. (2004). Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 7, 254–261. doi: 10.1016/j.pbi.2004.03.007 PubMed DOI

Gianoli E., Molina-Montenegro M. A. (2021). Evolution of physiological performance in invasive plants under climate change. Evolution 75, 3181–3190. doi: 10.1111/evo.14314 PubMed DOI

Girija A., Han J., Corke F., Brook J., Doonan J., Yadav R., et al. . (2022). Elucidating drought responsive networks in tef (Eragrostis tef) using phenomic and metabolomic approaches. Physiologia Plantarum. 174, e13597. doi: 10.1111/ppl.13597 PubMed DOI

Glaubitz U., Erban A., Kopka J., Hincha D.K., Zuther E.. (2015). High night temperature strongly impacts TCA cycle, amino acid and polyamine biosynthetic pathways in rice in a sensitivity-dependent manner. Journal of Experimental Botany. 66, 6385–6397. doi: 10.1093/jxb/erv352 PubMed DOI PMC

Hayat S., Hayat Q., Alyemeni M. N., Wani A. S., Pichtel J., Ahmad A. (2012). Role of proline under changing environments. Plant Signaling Behav. 7, 1456–1466. doi: 10.4161/psb.21949 PubMed DOI PMC

Ihsan M. Z., El-Nakhlawy F. S., Ismail S. M., Fahad S., Daur I. (2016). Wheat phenological development and growth studies as affected by drought and late season high temperature stress under arid environment. Front. Plant Sci. 7. doi: 10.3389/fpls.2016.00795 PubMed DOI PMC

IPCC (2018). Summary for policymakers- global warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. Masson-Delmotte V., Zhai P., Pörtner H.-O., Roberts D., Skea J., Shukla P.R., et al. (Geneva, Switzerland: World Meteorological Organization; )

Irfan M., Datta A. (2017). Improving food nutritional quality and productivity through genetic engineering. Int. J. Cell Sci. Mol. Biol. 2, 555576. doi: 10.19080/IJCSMB.2017.02.555576 DOI

Jagtap V., Bhargava S., Streb P., Feierabend J. (1998). Comparative effect of water, heat and light stresses on photosynthetic reactions in Sorghum bicolor (L.) moench. J. Exp. Bot. 49, 1715–1721. doi: 10.1093/jxb/49.327.1715 DOI

Jauregui I., Aroca R., Garnica M., Zamarreño Á.M., García-Mina J. M., Serret M. D., et al. . (2015). Nitrogen assimilation and transpiration: Key processes conditioning responsiveness of wheat to elevated [CO2] and temperature. Physiologia Plantarum. 155, 338–354. doi: 10.1111/ppl.12345 PubMed DOI

Jiang Y., Huang B. (2001). Drought and heat stress injury to two cool-season turfgrasses in relation to antioxidant metabolism and lipid peroxidation. Crop Sci. 41, 436–442. doi: 10.2135/cropsci2001.412436x DOI

Kahiluoto H., Kaseva J., Balek J., Olesen J. E., Ruiz-Ramos M., Gobin A., et al. . (2019). Decline in climate resilience of european wheat. Proc. Natl. Acad. Sci. United States America. 116, 123–128. doi: 10.1073/pnas.1804387115 PubMed DOI PMC

Khadka K., Earl H. J., Raizada M. N., Navabi A. (2020). A physio-morphological trait-based approach for breeding drought tolerant wheat. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.00715 PubMed DOI PMC

Kiani-Pouya A., Roessner U., Jayasinghe N. S., Lutz A., Rupasinghe T., Bazihizina N., et al. . (2017). Epidermal bladder cells confer salinity stress tolerance in the halophyte quinoa and atriplex species. Plant Cell Environ. 40, 1900–1915. doi: 10.1111/pce.12995 PubMed DOI

Kirschbaum M. U. F., McMillan A. M. S. (2018). Warming and elevated CO2 have opposing influences on transpiration. Which is more important? Curr. Forestry Rep. 4, 51–71. doi: 10.1007/s40725-018-0073-8 DOI

Klem K., Gargallo-Garriga A., Rattanapichai W., Oravec M., Holub P., Veselá B., et al. . (2019). Distinct morphological, physiological, and biochemical responses to light quality in barley leaves and roots. Front. Plant Sci. 10. doi: 10.3389/fpls.2019.01026 PubMed DOI PMC

Krasensky J., Jonak C. (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593–1608. doi: 10.1093/jxb/err460 PubMed DOI PMC

Kumari M., Joshi R., Kumar R. (2020). Metabolic signatures provide novel insights to picrorhiza kurroa adaptation along the altitude in Himalayan region. Metabolomics. 16, 77. doi: 10.1007/s11306-020-01698-8 PubMed DOI

Kumar R., Joshi R., Kumari M., Thakur R., Kumar D., Kumar S. (2020). Elevated CO2 and temperature influence key proteins and metabolites associated with photosynthesis, antioxidant and carbon metabolism in Picrorhiza kurroa . J. Proteomics. 219, 103755. doi: 10.1016/j.jprot.2020.103755 PubMed DOI

Kurepin L. V., Ivanov A. G., Zaman M., Pharis R. P., Hurry V., Hüner N. P. A. (2017). “Interaction of glycine betaine and plant hormones: protection of the photosynthetic apparatus during abiotic stress,” in Photosynthesis: Structures, mechanisms, and applications eds. Hou H., Najafpour M., Moore G, Allakhverdiev S. (Cham: Springer International Publishing; ), 185–202. doi: 10.1007/978-3-319-48873-8_9 DOI

Levine L. H., Kasahara H., Kopka J., Erban A., Fehrl I., Kaplan F., et al. . (2008). Physiologic and metabolic responses of wheat seedlings to elevated and super-elevated carbon dioxide. Adv. Space Res. 42, 1917–1928. doi: 10.1016/j.asr.2008.07.014 DOI

Li B., Fan R., Sun G., Sun T., Fan Y., Bai S., et al. . (2021). Flavonoids improve drought tolerance of maize seedlings by regulating the homeostasis of reactive oxygen species. Plant Soil. 461, 389–405. doi: 10.1007/s11104-020-04814-8 DOI

Li Y., Xu S., Wang Z., He L., Xu K., Wang G. (2018). Glucose triggers stomatal closure mediated by basal signaling through HXK1 and PYR/RCAR receptors in arabidopsis. J. Exp. Bot. 69, 1471–1484. doi: 10.1093/jxb/ery024 PubMed DOI PMC

Meehl G. A., Stocker T. F., Collins W. D., Friedlingstein P., Gaye A. T., Gregory J. M., et al. (2007). "Global climate projections," in Climate change 2007: The physical science basis. contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change, eds.Solomon S., Qin H. L. M. D., Manning M., Chen Z., Marquis M., Averyt K. B. (Cambridge, UK and New York, USA: Cambridge University Press; ).

Munné-Bosch S., Queval G., Foyer C. H. (2012). The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol. 161, 5–19. doi: 10.1104/pp.112.205690 PubMed DOI PMC

Naing A. H., Kim C. K. (2021). Abiotic stress-induced anthocyanins in plants: Their role in tolerance to abiotic stresses. Physiologia Plantarum. 172, 1711–1723. doi: 10.1111/ppl.13373 PubMed DOI

Nuttall J. G., Barlow K. M., Delahunty A. J., Christy B. P., O’Leary G. J. (2018). Acute high temperature response in wheat. Agron. J. 110, 1296–1308. doi: 10.2134/agronj2017.07.0392 DOI

Obata T., Fernie A. R. (2012). The use of metabolomics to dissect plant responses to abiotic stresses. Cell. Mol. Life Sci. 69, 3225–3243. doi: 10.1007/s00018-012-1091-5 PubMed DOI PMC

Obata T., Witt S., Lisec J., Palacios-Rojas N., Florez-Sarasa I., Araus J. L., et al. . (2015). Metabolite profiles of maize leaves in drought, heat and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol. 169, 2665–2683. doi: 10.1104/pp.15.01164 PubMed DOI PMC

Pandey P., Irulappan V., Bagavathiannan M. V., Senthil-Kumar M. (2017). Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.00537 PubMed DOI PMC

Pandey P., Ramegowda V., Senthil-Kumar M. (2015). Shared and unique responses of plants to multiple individual stresses and stress combinations: Physiological and molecular mechanisms. Front. Plant Sci. 6. doi: 10.3389/fpls.2015.00723 PubMed DOI PMC

Pang Z., Chong J., Zhou G., de Lima Morais D. A., Chang L., Barrette M., et al. . (2021). MetaboAnalyst 5.0: Narrowing the gap between raw spectra and functional insights. Nucleic Acids Res. 49, W388–W396. doi: 10.1093/nar/gkab382 PubMed DOI PMC

Peng M., Shahzad R., Gul A., Subthain H., Shen S., Lei L., et al. . (2017). Differentially evolved glucosyltransferases determine natural variation of rice flavone accumulation and UV-tolerance. Nature Communications. 8, 1975. doi: 10.1038/s41467-017-02168-x PubMed DOI PMC

Ren S., Ma K., Lu Z., Chen G., Cui J., Tong P., et al. . (2019). Transcriptomic and metabolomic analysis of the heat-stress response of Populus tomentosa Carr. Forests. 10, 383. doi: 10.3390/f10050383 DOI

Reyenga P. J., Howden S. M., Meinke H., Hall W. B. (2001). Global change impacts on wheat production along an environmental gradient in south Australia. Environ. Int. 27, 195–200. doi: 10.1016/S0160-4120(01)00082-4 PubMed DOI

Rice-Evans C., Miller N., Paganga G. (1997). Antioxidant properties of phenolic compounds. Trends Plant Sci. 2, 152–159. doi: 10.1016/S1360-1385(97)01018-2 DOI

Rizhsky L., Liang H., Shuman J., Shulaev V., Davletova S., Mittler R. (2004). When defense pathways collide. The response of arabidopsis to a combination of drought and heat stress. Plant Physiol. 134, 1683–1696. doi: 10.1104/pp.103.033431 PubMed DOI PMC

Rosa M., Prado C., Podazza G., Interdonato R., González J. A., Hilal M., et al. . (2009). Soluble sugars. Plant Signaling Behav. 4, 388–393. doi: 10.4161/psb.4.5.8294 PubMed DOI PMC

Sardans J., Gargallo-Garriga A., Urban O., Klem K., Walker T. W. N., Holub P., et al. . (2020). Ecometabolomics for a better understanding of plant responses and acclimation to abiotic factors linked to global change. Metabolites. 10, 239. doi: 10.3390/metabo10060239 PubMed DOI PMC

Sharma M., Irfan M., Kumar A., Kumar P., Datta A. (2021). “Recent insights into plant circadian clock response against abiotic stress,” Journal of Plant Growth Regulation. 221, 112403. doi: 10.1007/s00344-021-10531-y DOI

Sharma M., Kumar P., Verma V., Sharma R., Bhargava B., Irfan M. (2022). Understanding plant stress memory response for abiotic stress resilience: Molecular insights and prospects. Plant Physiol. Biochem. 179, 10–24. doi: 10.1016/j.plaphy.2022.03.004 PubMed DOI

Shewry P. R. (2009). Wheat. J. Exp. Bot. 60, 1537–1553. doi: 10.1093/jxb/erp058 PubMed DOI

Sicher R. (2013). Combined effects of CO2 enrichment and elevated growth temperatures on metabolites in soybean leaflets: Evidence for dynamic changes of TCA cycle intermediates. Planta. 238, 369–380. doi: 10.1007/s00425-013-1899-8 PubMed DOI

Šigut L., Holisova P., Klem K., Prtova M., Calfapietra C., Marek M. V., et al. (2015). Does long-term cultivation of saplings under elevated CO2 concentrationinfluence their photosynthetic response to temperature? Ann. Bot. 116, 929–939. doi: 10.1093/aob/mcv043 PubMed DOI PMC

Soba D., Ben Mariem S., Fuertes-Mendizábal T., Méndez-Espinoza A. M., Gilard F., González-Murua C., et al. . (2019). Metabolic effects of elevated CO2 on wheat grain development and composition. J. Agric. Food Chem. 67, 8441–8451. doi: 10.1021/acs.jafc.9b01594 PubMed DOI

Tahjib-Ul-Arif M., Zahan M. I., Karim M. M., Imran S., Hunter C. T., Islam M. S., et al. . (2021). Citric acid-mediated abiotic stress tolerance in plants. Int. J. Mol. Sci. 7235. doi: 10.3390/ijms22137235 PubMed DOI PMC

Templer S. E., Ammon A., Pscheidt D., Ciobotea O., Schuy C., McCollum C., et al. . (2017). Metabolite profiling of barley flag leaves under drought and combined heat and drought stress reveals metabolic QTLs for metabolites associated with antioxidant defense. J. Exp. Bot. 68, 1697–1713. doi: 10.1093/jxb/erx038 PubMed DOI PMC

Thornton P. K., Ericksen P. J., Herrero M., Challinor A. J. (2014). Climate variability and vulnerability to climate change: A review. Global Change Biol. 20, 3313–3328. doi: 10.1111/gcb.12581 PubMed DOI PMC

Trovato M., Funck D., Forlani G., Okumoto S., Amir R. (2021). Editorial: Amino acids in plants: Regulation and functions in development and stress defense. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.772810 PubMed DOI PMC

Walkowiak S., Gao L., Monat C., Haberer G., Kassa M. T., Brinton J., et al. . (2020). Multiple wheat genomes reveal global variation in modern breeding. Nature. 588, 277–283. doi: 10.1038/s41586-020-2961-x PubMed DOI PMC

Wu G., Johnson S. K., Bornman J. F., Bennett S. J., Clarke M. W., Singh V., et al. . (2016). Growth temperature and genotype both play important roles in sorghum grain phenolic composition. Sci. Rep. 6, 21835. doi: 10.1038/srep21835 PubMed DOI PMC

Xalxo R., Yadu B., Chandra J., Chandrakar V., Keshavkant S. (2020). “Alteration in carbohydrate metabolism modulates thermotolerance of plant under heat stress,” in Heat stress tolerance in plants eds. Wani S.H., Kumar V. (New Jersey, USA: Wiley; ), 77–115. doi: 10.1002/9781119432401.ch5 DOI

Xu G., Cao J., Wang X., Chen Q., Jin W., Li Z., et al. . (2019). Evolutionary metabolomics identifies substantial metabolic divergence between maize and its wild ancestor, teosinte. Plant Cell. 31, 1990–2009. doi: 10.1105/tpc.19.00111 PubMed DOI PMC

Zandalinas S. I., Balfagón D., Gómez-Cadenas A., Mittler R. (2022). Plant responses to climate change: Metabolic changes under combined abiotic stresses. J. Exp. Bot. 73, 3339–3354. doi: 10.1093/jxb/erac073 PubMed DOI

Zandalinas S. I., Mittler R. (2022). Plant responses to multifactorial stress combination. New Phytol. 234, 1161–1167. doi: 10.1111/nph.18087 PubMed DOI

Zandalinas S. I., Mittler R., Balfagón D., Arbona V., Gómez-Cadenas A. (2018). Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum. 162, 2–12. doi: 10.1111/ppl.12540 PubMed DOI

Zinta G., AbdElgawad H., Peshev D., Weedon J. T., Van den Ende W., Nijs I., et al. . (2018). Dynamics of metabolic responses to periods of combined heat and drought in arabidopsis thaliana under ambient and elevated atmospheric CO2 . J. Exp. Bot. 69, 2159–2170. doi: 10.1093/jxb/ery055 PubMed DOI PMC